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Telopea 12(1) 47–58
From populations to communities:
understanding changes in rainforest diversity
through the integration of molecular, ecological
and environmental data
Maurizio Rossetto 1,2
National Herbarium of NSW, Botanic Gardens Trust, Mrs Macquaries road, Sydney NSW 2000
Address for correspondence: [email protected]
2
School of Environmental Sciences and Natural Resource Management, University of New
England, Armidale NSW 2351
1
Abstract
The progressive aridification of the Australian continent during the last 30 million years has
considerably reduced the amount of habitat suited to broad-leaved vegetation. The fossil
record suggests that much diversity has been lost in that period, and that the extreme climatic
fluctuations of the Quaternary stressed the remaining refugial areas even further. Yet, despite the
considerable transformation of the surrounding environment, the rainforest remnants scattered
along the east coast still contain considerable levels of biodiversity and endemism. This complex
matrix of remnants reflects a long and varied history of selective pressures, and represents an ideal
setting for evolutionary studies. Although the conservatism of some rainforest lineages points
to localised environmental stability, it also highlights the importance of adaptive potential and
selective tolerance. A number of recent case studies show that the tension between persistence
and dispersal (often in combination with other factors) is an important mechanism contributing
to the survival and distribution of rainforest species. This paper discusses the benefits of linking
molecular, ecological and environmental data to improve both interpretations and hypotheses
of current (neo) and past (paleo) distributions and relationships among rainforest plants,
and how this information can be used to improve conservation and management approaches.
Understanding how species and communities have survived past environmental change will be
a critical step in predicting likely responses to future threats. A selection of integrative research
topics that are likely to increase our predictive capacity for future change are outlined.
Paper from the Australian Systematic Botany Society Conference held
in Cairns, November 2006
© 2008 Royal Botanic Gardens and Domain Trust
ISSN0312-9764
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Telopea 12(1): 2008
Rossetto
Introduction: decline from dominance
Paleo-botanical studies suggest that during the Mid Eocene, closed canopy forests
represented the dominant vegetation type across the Australian continent (Kershaw
et al. 1991). Forests similar to those now restricted to the northern and wetter parts of
Queensland were once widespread at much higher latitudes. As the Australian landmass separated from Antarctica in the Late Eocene, the formation of circumpolar
currents increased the amount of moisture trapped at the South Pole as ice. This was
followed by a global decline in temperature, and by increased aridification and retreat
of rainforest vegetation continent-wide (Greenwood & Christophel 2005). By the
Mid Miocene the extensive Western Australian paleo-drainage had dried. Rainforests
disappeared from central Australia and were eventually restricted to wetter coastal
habitats by the Late Miocene (Martin 2006). Evidence suggests that in the last 10 My
the core rainforest areas of the Wet Tropics have remained relatively ecologically stable,
while further fragmentation, aridification and loss of biodiversity took place at more
southern latitudes (Kershaw et al. 2005).
Extensive macro- and micro-fossil records show that the Mid Eocene forests were
dominated by families (such as Cunoniaceae, Elaeocarpaceae, Lauraceae, Myrtaceae
and Proteaceae) that remain important in modern Australia (Greenwood &
Christophel 2005). Floristically, rainforests are often considered as the living links to
Australia’s ancient past as they harbour a high concentration of primitive angiosperms
(Webb & Tracey 1981). These paleo-endemics are vestiges of previously widespread
taxa and are concentrated in the Wet Tropics and across the eastern border between
Queensland and New South Wales (Whiffin & Hyland 1986). In some families only
moderate morphological modifications have occurred during the last 55 My despite
the major climatic adjustments that took place as the Australian continent traveled
through 20° in latitude (Hill 2004). However, while some lineages have barely changed
in morphology, the fossil record proves that their distribution has been considerably
modified. For example, Oligocene and Miocene fossil floras from Victoria, New South
Wales and southern and central Queensland contain endocarps of Elaeocarpus clarkei
F.Muell. morphologically similar to the modern E. bancroftii F.Muell. & F.M.Bailey
that is restricted to the Wet Tropics (Rozefelds & Christophel 1996, Greenwood &
Christophel 2005).
Interestingly, the morphological adjustments that did take place were not necessarily in
response to aridification. Hill (2004) suggested that the appearance of scleromorphy/
xeromorphy in Proteaceae during the Mid Eocene (a period of high rainfall) was likely to
be a response to nutrient deficient soils and/or higher light levels. These characteristics
however, were an important source of evolutionary potential for adaptation to aridity,
with increased diversification of sclerophyllous lineages taking place between 25
and 10 Mya (Crisp et al. 2004). More recently, molecular phylogenetic studies have
contributed to the development of new hypotheses about previously unexpected
relationships between dry-adapted and rainforest lineages. One such example is
Tremandraceae, a former southern family of dry-adapted shrubs recently shown to be
part of Elaeocarpaceae (comprising mostly rainforest trees), with the diversification of
Tetratheca, the largest genus, putatively occurring during the major aridification phase
of the Late Miocene (Crayn et al. 2006).
Because of the continental-scale climatic and environmental changes described, all
remaining rainforest areas in Australia can be considered as refugia. Yet, despite covering
Integrative studies on flora evolution Telopea 12(1): 2008
49
<1% of the land area, rainforests still contain a considerable portion of Australia’s
unique biodiversity (Adam 1992).
The extreme climatic events of the Quaternary
The fossil record suggests that the greatest reduction in suitable rainforest habitat and
diversity occurred before the Quaternary (Hill 2004). However, the most recent ice-age
caused significant adjustments to species distributions worldwide, particularly during
the last 700 Ky when climatic fluctuations were more intense (Hays et al. 1976). In
Australia, rather than creating extensive ice sheets, ice-ages shaped the distribution
of vegetation by increasing aridity, fire frequency and fire intensity (Bowman 2000).
Paleo-climatic models suggest that the changes in temperature and moisture regimes
caused by glacial maxima fragmented rainforest remnants into even smaller refugia
(Nix 1991). As in most other areas around the globe, some species adapted to these
new conditions or dispersed to more suitable locations, while others only persisted in
marginal portions of their former range or became extinct (Hewitt 2000). Well-dated
marine palynological records from northern Queensland suggest that throughout the
late Cenozoic, complex rainforests occupied the wetter habitats and were surrounded by
extensive drier araucarian forests that functioned as a transition to true sclerophyllous
vegetation (Kershaw et al. 2005). In the last 200 Ky, increased climatic instability
brought about greater environmental stress and vulnerability to fire, resulting in the
replacement of the araucarian forest by true sclerophyllous vegetation dominated by
eucalypts. The last glacial maximum was particularly intense, with severe and persistent
fragmentation revealed by Eucalyptus intrusions in current Wet Tropics rainforest areas
as recently as eight thousand years ago (Hopkins et al. 1993). The intensity of these
more recent events is likely to have caused further extinctions (Kershaw 1994).
During the brief inter-glacials (such as the one we are currently in) climatic conditions
improved and refugial populations could expand into newly available habitat. The
success of post-glacial expansions depended on a range of factors such as recruitment
and dispersal potential, and played an important role in defining modern-day
distribution patterns. Extensive palynological records from the Northern Hemisphere
show that tree species responded differently to climate change, tracking their individual
habitat requirements according to their dispersal capability (Hewitt 1996). During this
expansion process, transitional plant communities that were considerably different to
current ones were established with the help of small populations that persisted within
microclimate pockets in areas otherwise considered as unsuitable. Recent studies
suggest that a predicted loss of ‘core’ habitat does not necessarily imply population
extinction (although it certainly implies greater vulnerability), and that in order to
understand temporal distributional changes of plant communities, it is essential to
appreciate the tolerance of single species to environmental fluctuations (Stewart &
Lister 2001). Similar species-level palynological records have not yet been identified for
the Australian paleo-flora, as the focus of most studies has been on broad vegetation
structure. As we await more detailed palynological investigations on rainforest taxa,
we can assume that suitable circumstances existed for the survival of small refugial
populations along the eastern coast of Australia.
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Rossetto
The molecular revolution: fine-scale evolutionary dynamics
Paleo-ecological, biogeographic and systematic studies have provided valuable
information on the evolutionary and distributional shifts that shaped the Australian
flora. However, if we are interested in the factors impacting on the survival/extinction
of species, we must also consider the fine-scale influence of selective biotic and abiotic
processes. The advances in molecular genetics over the past 20 years have significantly
contributed to this goal. For example, reciprocally monophyletic populations
(evolutionary significant units) can be identified by sampling selected loci prone to
high substitution rates but non-recombinant and uni-parentally inherited (Moritz
1994). These genetically distinct groups identify historically isolated populations and
define the location of barriers to gene flow (such as those established by changing
climatic conditions). The availability of complementary fossil and molecular data and
the recent development of improved analytical approaches (Sanderson 2003) provide
the opportunity to explore the temporal dimension of these evolutionary processes.
Comparative studies on co-distributed species can make use of the genetic signatures
left by different expansion patterns to identify the locations of refugia, the factors
affecting expansion patterns and the adaptive potential of these taxa. In the Northern
Hemisphere, haplotypic data from a range of maternally-inherited chloroplast loci
have been used to track post-glacial re-colonisation patterns in a considerable number
of tree species, confirming models previously suggested by palynological data (Petit et
al. 2005). Interestingly, comparative studies in Quercus have concluded that during the
last glaciation a more complex matrix of localised refugia (and consequently greater
genetic diversity) was maintained in California than in Western Europe, highlighting
how habitat availability and different life-history combinations can influence recolonisation outcomes (Grivet et al. 2006). Similar studies are still limited in Australia.
An overview of plastid DNA variation across the natural range of Tasmanian eucalypts
from section Maidenaria showed that genetic variation correlates more with geography
than taxonomy (McKinnon et al. 2001). This regional haplotype-sharing pattern
suggests that extensive hybridisation took place among local eucalypts following
the latest ice age (McKinnon et al. 2004), a pattern reminiscent of that found in the
European oaks (Petit et al. 2002).
An Australian rainforest perspective
Australian rainforest habitats provide an ideal setting for evolutionary studies (Schneider
et al. 1998). They have high amounts of taxonomic diversity and endemism and, as
suggested by fossil evidence, include ancient lineages that have been continuously
present in the region (Hill 2004, Greenwood & Christophel 2005). Furthermore,
rainforests are currently distributed across a matrix of differentially sized and spaced
remnants that reflect a long and varied history of environmental disturbance and
selective pressures (Moritz & McDonald 2005).
Until recently, most of the molecular research investigating the history and dynamics
of Australian rainforests was focused on the fauna of the Wet Tropics. Phylogeographic
studies on a number of low-vagility vertebrates (including habitat-specialist birds,
lizards and frogs) detected significant genetic disjunction between populations
distributed across a previously identified (Nix 1991) biogeographic barrier, the Black
Mountain Corridor (BMC, a strip of low-lying land between Cairns and Mossman that
Integrative studies on flora evolution Telopea 12(1): 2008
51
interrupts the Great Dividing Range; Schneider et al. 1998). Molecular divergence was
ascribed to multiple vicariance episodes mostly near the BMC area, with the majority
of speciation events originating before the Pleistocene. This suggests that the climatic
fluctuations of the Quaternary generally emphasised existing divergence patterns
rather than creating new ones (Schneider et al. 1998, Schneider & Williams 2005). The
shallow genetic divergences measured between single putative refugia, and the lower
genetic diversity in southern populations also suggest that a loss of suitable habitat
during glacial maxima (and likely decline in species richness) was followed by rapid recolonisation (Moritz & McDonald 2005). As these events are affected by the ecological
characteristics of each species, it has been suggested that future studies should also
pay attention to the ecological factors likely to impart selective constraints rather than
focus on geographic isolation alone (Schneider et al. 1999).
The available fossil evidence from the Australian rainforest flora also points to an
historical decline in diversity, although limited examples of recent speciation exist within
southern rainforests (Rossetto 2005, Savolainen et al. 2006). To date, no phylogeographic
research on the Australian rainforest flora has been published. However, a few studies
assessing overall genetic diversity across single species have detected significant north/
south genetic disjunctions (Fontainea australis Jessup & Guymer, Rossetto et al. 2000;
Araucaria bidwillii Hook., Pye & Gadek 2004; Nothofagus moorei (F.Muell.) Krasser,
Taylor et al. 2005). A more recent study sampled the entire distribution of two related
and co-distributed rainforest trees, documenting substantial discrepancies in genetic
differentiation across biogeographic barriers such as the BMC (Rossetto et al. 2007).
While Elaeocarpus largiflorens C.T.White revealed an abrupt genetic front between
two morphologically distinct subspecies separated by the BMC, the same barrier was
inconsequential to E. angustifolius Blume (which showed lower genetic differentiation
across a much wider geographic gap). A broader study in progress is comparing genetic
disjunctions across 11 tropical Elaeocarpus species representing a range of habitat
preferences and life-history traits combinations. Interesting preliminary patterns
include north/south genetic disjunctions for higher-altitude species (as previously
shown in E. largiflorens), as well as an unexpected lack of impact of fruit type on genetic
structure (Rossetto et al. in prep.).
Understanding evolutionary patterns at temporal and geographical scales is only the first
step as it is essential to relate these patterns to causal factors. Simulations investigating
the expansion potential of trees show that models that take into account life-history
traits relating to dispersal and life-cycle are more realistic and more likely to provide
the correct interpretation of molecular data (Austerlitz & Garnier-Gere 2003). Thus
in order to discover the factors regulating landscape connectivity, it is important to
develop more studies targeting range-wide sampling across related species representing
diverse habitat preferences and life-history traits.
Evolutionary ecology: finding meaningful patterns
Multi-species studies integrating ecological, molecular and environmental evidence
can identify broad evolutionary patterns, and recognise the mechanisms that influence
the survival of populations and species. Recent work is uncovering broad correlations
between life-history traits and the distribution of taxa. For instance, a study comparing
sexual systems across Australian tropical trees (1113 species from 83 families) found
that the incidence of monoecy is significantly higher in Australia than in other tropical
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Rossetto
floras (Gross 2005). Although phylogeny might be partly responsible for this (about
50% of the monoecious taxa are from two families), Gross (2005) suggested that the
reliance on inefficient insect pollinators could have favoured the maintenance of
monoecy. Another large-scale rainforest study including 258 species from the Nightcap
Ranges (northern NSW), identified the life-history traits associated with persistence
and dispersal as the most influential in describing the current distribution of locally
rare trees (Rossetto & Kooyman 2005). The results suggest that major environmental
changes have been important selective drivers on large-fruited species within these
southern rainforests. It can be assumed that while large-seeded plants can establish
more efficiently, lower seed production and the absence of dispersal organisms reduce
expansion capability after a bottleneck. As a result, the large-fruited species that survived
habitat contractions are likely to be the ones that could enhance their competitiveness
through in-ground stem persistence. Fine-scale molecular studies on narrow endemic
taxa are supporting this hypothesis (Rossetto et al. 2004a, Rossetto & Kooyman 2005,
Rossetto et al. in prep.). For instance, the high levels of diversity within small, isolated
populations of Eidothea hardeniana P.H.Weston and Elaeocarpus sedentarius could be
symptomatic of a strategy involving the reliance on self-replacement of individuals
through resprouting rather than recruitment. The lack of correlation between genetic
and geographic disjunctions despite the presence of strong population-level genetic
autocorrelation, also highlight the impact of limited dispersal.
The persistence niche
The importance of persistence is often neglected while that of recruitment is emphasised,
yet many ecosystems are dominated by resprouters (Bond & Midgley 2001). Vegetative
reproduction provides a competitive edge by allowing the sharing of resources between
connected ramets, and can be considered as an alternative lifecycle loop that allows
persistence in species that are not able to complete a normal life-cycle. The persistence
niche is suitable to a range of disturbance regimes, enables species to tolerate long
periods without recruitment, allows regeneration in unsuitable conditions and can
reduce the loss of population-level genetic diversity (Bond & Midgley 2001). This
strategy can be particularly suitable to species constrained to less than ideal habitats,
and Johnson and Lacey (1983) suggested that it might be an important long-term
survival strategy for rainforest trees.
Resprouting is a relatively safe escape route under suboptimal conditions but prolonged
clonal growth through environmental suppression of sexual reproduction can lead to
monoclonal populations. There are some interesting examples of extreme clonality in
the Australian flora. For example a range of molecular approaches could not identify any
variation across individuals of Wollemia nobilis sampled from all known sites (Peakall et
al. 2003). Similar circumstances were discovered for Elaeocarpus williamsianus Guymer,
a tree restricted to a number of disjunct and mostly disturbed rainforest remnants in
northern NSW. A genetic study found that all populations but one consisted of single
clones and since this is a preferential outcrossing species, viable seed could not be set
(Rossetto et al. 2004a). E. williamsianus is now locked into an evolutionary dead-end
loop: long- and short-term disturbance events have favoured excessive clonality that
prevents sexual reproduction and long distance dispersal. In turn, limited dispersal
prevents range expansion and the potential gene flow which would re-establish a
balance between vegetative and sexual reproduction.
Integrative studies on flora evolution Telopea 12(1): 2008
53
The importance of dispersal
There is increasing evidence that expansion mechanism and habitat preference are
among the main factors affecting the temporal distribution and the diversification
potential of plant species (Pearson 2006). Dispersal of propagules enables genetic
exchange (thus reducing vicariant divergence and inbreeding), as well as expansion to
newly available habitat and recovery after unfavourable circumstances. For instance,
rainforest trees that produce fleshy, highly dispersible fruits can be expected to have lower
levels of between-population genetic differentiation than species with less palatable
fruits (Shapcott 2000). Thus fruit morphology can affect current distribution patterns,
and mal-adaptation through lack of dispersers can explain rarity in the vertebrate-poor
rainforests of northern NSW (Rossetto et al. 2004a, Rossetto & Kooyman 2005, Rossetto
et al. submitted), although it does not imply short-term extinction (as previously
suggested; Archer et al. 1994). It is important to remember that inference of expansion
potential from fruit morphology alone can be unsatisfactory, as capacity for dispersal
is not necessarily synonymous with effective dispersal (i.e. including establishment).
Unfortunately, information on dispersal efficiency of the Australian rainforest flora is
still limited although an increasing number of recent studies are measuring active fruit
dispersal by Wet Tropic frugivores (Westcott & Graham 2000, Westcott et al. 2005).
The tension between persistence and dispersal is likely to be an important mechanism
contributing to the current distribution of many rainforest species, but clearly there are
other factors that also need to be investigated.
These early studies are showing that paleo-endemic species can survive for a long
time within small populations (Rossetto et al. 2000, Rossetto et al. 2004a, Rossetto
& Kooyman 2005). This suggests that single populations, or even whole new species
(Weston & Kooyman 2002), can still be found within moderately-sized vegetation
remnants, and that small populations are not doomed as they can persist and maintain
potential for future expansion (if and when suitable conditions arise). However, it is
important to stress that this apparent resilience does not make restricted populations
less vulnerable to stochastic events and anthropogenic disturbance.
Reacting to the biodiversity crisis
During the last 150 years the impact of logging, clearing and urbanisation has further
reduced the extent of rainforest vegetation in Australia (Connelly & Specht 1988). This
is particularly true for the Big Scrub of northern NSW (which covered an area of over
70 000 ha prior to European settlement) where widespread clearing has restricted
rainforest vegetation to approximately 1% of its original distribution (Lott & Duggin
1993). Rainforests worldwide are subject to increasing external pressures and degradation
that dissect continuous species distributions into isolated fragments (Whitmore 1997,
Arnold & Rossetto 2002, Rossetto et al. 2004b) and despite recent controversy on the
true extent of the global rainforest biodiversity crisis (Wright & Muller-Landau 2006;
but see Laurence 2006), we now recognise that drastic environmental modifications
linked to impending climate change threaten the integrity and long-term sustainability
of rainforest ecosystems. For instance, in the Wet Tropics where the altitudinal gradient
is the most significant factor explaining fauna compositional patterns (Williams et al.
2003), climate change scenarios (with temperature increasing up to 5°C in the short
term) predict a significant reduction in suitable upland conditions and the potential
disappearance of entire habitat types. Consequently, rainforest conservation and
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Rossetto
management faces challenges at two temporal levels: the contemporary, dealing with
current threatened species lists and habitat fragmentation, and the future, dealing with
the predicted decline of already small habitat remnants.
Understanding likely responses to future threats is crucial to conservation planning, and
one of the main challenges for conservation biology will be to anticipate environmental
change and adjust management approaches accordingly. By appreciating how past
climatic cycles have affected selective biotic and abiotic pressures and consequently
the survival and distribution of species and ecological communities, we will be able
to develop predictive models that determine vulnerability to future change. An
increasingly common response to the problem is the development of multi-species
recovery plans, which hopefully will be followed by multi-species implementation
projects. Biologically meaningful multi-species approaches are being explored, such
as the one based on trait-based functional groups currently being developed for the
threatened flora of the Border Ranges (Kooyman & Rossetto in prep.). In the longterm, a focused approach involving integrative research will facilitate the management
of threats and risks at the species, multi-species and the ecosystem levels.
Conclusion: where to from here?
Fossil evidence shows a considerable level of conservatism in the Australian rainforest
flora despite gradual long-term and intensive short-term environmental change. This
suggests the presence of localised environmental stability, but also points to the adaptive
potential of some lineages that have survived the evolutionary sifting of severe climatic
cycles. It can be expected that a range of key biological (evolutionary) factors played an
important role in the endurance of the remaining rainforest flora. To better understand
the factors influencing evolutionary processes, future research should include:
1) P
hylogenetically structured multi-species molecular ecology studies targeting
important biogeographic barriers and selected functional groups. The discovery of
repeated patterns of genetic divergence will identify landscape features of evolutionary
significance and selectively important life-history traits. The availability of relevant
paleo-ecological data would also enable the accurate dating of these events.
2) E
valuations of multiple associative patterns among selected life-history traits and the
distribution of species (and/or genes). This will contribute to the identification of the
major factors likely to affect the evolutionary response to changing environmental
circumstances.
3) T
he development of models (based on appropriate levels of ground-truthing and
in-situ data gathering) that can differentiate between potential and realised niches
for species and ecological communities. This will improve our understanding of the
level of tolerance of species and communities, and enable us to predict the impact of
future environmental and climatic change.
On their own, these are important areas of research but the greatest scientific benefit
will arise from developing experimental designs that combine them all. The Australian
rainforest flora provides a unique evolutionary scenario for this type of research;
however these approaches are suitable and relevant to a broad range of vegetation types.
Integrative studies on flora evolution Telopea 12(1): 2008
55
Acknowledgments
I would like to thank Darren Crayn, Robert Kooyman and the editorial committee for
providing useful comments on this manuscript.
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Manuscript received 15 April 2007, accepted 30 August 2007